Loss of function of bHLH transcription factor Nrd1 in tomato induces an arabinogalactan protein-encoding gene and enhances resistance toPseudomonas syringaepv.tomato

Basic helix-loop-helix (bHLH) transcription factors constitute a superfamily in eukaryotes but their roles in plant immunity remain largely uncharacterized. We found that the transcript abundance in tomato leaves of one bHLH transcription factor-encoding gene,Nrd1(negativeregulator of resistance toDC30001), was significantly increased after treatment with the immunity-inducing flgII-28 peptide. Plants carrying a loss-of-function mutation inNrd1(Λnrd1) showed enhanced resistance toPseudomonas syringaepv.tomato(Pst) DC3000 although early pattern-triggered immunity responses such as generation of reactive oxygen species and activation of mitogen-activated protein kinases after treatment with flagellin-derived flg22 and flgII-28 peptides were unaltered compared to wild-type plants. An RNA-Seq analysis identified a gene,Agp1, whose expression is strongly suppressed in anNrd1-dependent manner.Agp1encodes an arabinogalactan protein and overexpression of theAgp1gene inNicotiana benthamianaled to ∼10-fold lessPstgrowth compared to the control. These results suggest that the Nrd1 protein promotes tomato susceptibility toPstby suppressing the defense geneAgp1. RNA-Seq also revealed that loss of Nrd1 function has no effect on the transcript abundance of immunity-associated genes includingBti9, Core, Fls2, Fls3andWak1uponPstinoculation, suggesting that the enhanced immunity observed in the Δnrd1 mutants is due to the activation of key PRR signaling components as well as loss of Nrd1-regulated suppression ofAgp1.